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Marine Drugs marine drugs Article Structure and In Vitro Bioactivity against Cancer Cells of the Capsular Polysaccharide from the Marine Bacterium Psychrobacter marincola Maxim S. Kokoulin 1,* , Alexandra S. Kuzmich 1, Lyudmila A. Romanenko 1, Irina V. Chikalovets 1,2 and Oleg V. Chernikov 1 1 G.B. Elyakov Pacific Institute of Bioorganic Chemistry, Far Eastern Branch, Russian Academy of Sciences, 159/2, Prospect 100 let Vladivostoku, Vladivostok 690022, Russia; [email protected] (A.S.K.); [email protected] (L.A.R.); [email protected] (I.V.C.); [email protected] (O.V.C.) 2 Far Eastern Federal University, 8, Sukhanova str., Vladivostok 690950, Russia * Correspondence: [email protected]; Fax: +7-4232-314050 Received: 30 April 2020; Accepted: 18 May 2020; Published: 19 May 2020 Abstract: Psychrobacter marincola KMM 277T is a psychrophilic Gram-negative bacterium that has been isolated from the internal tissues of an ascidian Polysyncraton sp. Here, we report the structure of the capsular polysaccharide from P. marincola KMM 277T and its effect on the viability and colony formation of human acute promyelocytic leukemia HL-60 cells. The polymer was purified by several separation methods, including ultracentrifugation and chromatographic procedures, and the structure was elucidated by means of chemical analysis, 1-D, and 2-D NMR spectroscopy techniques. It was found that the polysaccharide consists of branched hexasaccharide repeating units containing two 2-N-acetyl-2-deoxy-d-galacturonic acids, and one of each of 2-N-acetyl-2-deoxy-d-glucose, d-glucose, d-ribose, and 7-N-acetylamino-3,5,7,9-tetradeoxy-5-N-[(R)-2-hydroxypropanoylamino]- l-glycero-l-manno-non-2-ulosonic acid. To our knowledge, this is the first finding a pseudaminic acid decorated with lactic acid residue in polysaccharides. The biological analysis showed that the capsular polysaccharide significantly reduced the viability and colony formation of HL-60 cells. Taken together, our data indicate that the capsular polysaccharide from P. marincola KMM 277T is a promising substance for the study of its antitumor properties and the mechanism of action in the future. Keywords: marine bacteria; Psychrobacter; capsular polysaccharide; pseudaminic acid; lactic acid; antiproliferative activity; HL-60 1. Introduction Many marine bacteria can produce extracellular polysaccharides (EPSs). Bacterial EPSs usually occur in two forms: As capsular polysaccharides (CPSs), if they are associated with the cell surface, and medium-released polysaccharides (MRPs), if they are completely released in the environment [1]. The presence of these biopolymers indicates their specific properties and functions that are beneficial to microorganisms; they play an essential role in protecting the bacterial cell from harsh environmental conditions (salinity, temperature, and the availability of nutrients), in surface adhesion (usually through the biofilms formation), intercellular signal transduction, and in resisting the host’s immune response. All these features help to survive and protect their producers from the complex marine environment [1,2]. Bacterial EPSs are bioglycans, mainly consisting of different monosaccharides or its derivatives. In addition, various types of organic and inorganic substituents (amino acids, acetates, pyruvates, Mar. Drugs 2020, 18, 268; doi:10.3390/md18050268 www.mdpi.com/journal/marinedrugs Mar. Drugs 2020, 18, 268 2 of 17 Mar. Drugs 2020, 18, x 2 of 17 lactates, phosphates, and sulfates) can decorate the main linear or branched polysaccharide chain [1,2]. [1,2]Such. aSuch high a degree high ofdegree variability of variability implies theimplies existence the ofexistence a huge numberof a huge of bacterial number polysaccharides, of bacterial polysaccharides,in which structural in which changes structural are almost changes unlimited. are almost unlimited. In recent decades, the growing demand for natural carbohydrate polymers for industrial use has In recent decades, the growing demand for natural carbohydrate polymers for industrial use has led to significant interest in polysaccharides produced by microorganisms. Additionally, EPSs from led to significant interest in polysaccharides produced by microorganisms. Additionally, EPSs from marine bacteria have prominent biological activity, including immunomodulatory, antiviral, as well marine bacteria have prominent biological activity, including immunomodulatory, antiviral, as well as as antitumor activities [3–5]. antitumor activities [3–5]. The genus Psychrobacter belongs to the class Gammaproteobacteria and includes both The genus Psychrobacter belongs to the class Gammaproteobacteria and includes both psychrophilic psychrophilic and psychrotolerant, halotolerant, and Gram-negative bacteria, which are associated and psychrotolerant, halotolerant, and Gram-negative bacteria, which are associated primarily with the primarily with the Antarctic and marine habitats [6]. Members of Psychrobacter have been isolated Antarctic and marine habitats [6]. Members of Psychrobacter have been isolated from various sources, from various sources, including the Antarctic sea ice, permafrost, marine sediments, deep and surface including the Antarctic sea ice, permafrost, marine sediments, deep and surface seawater, fish, and marine seawater, fish, and marine invertebrates. Several species have also been isolated from food, clinical sources,invertebrates. poultry Several, and livestock species have [7]. At also the been time isolated of writing, from the food, genus clinical Psychrobacter sources, poultry, comprises and 41 livestock validly [7]. Atdescribed the time species of writing, [8]. the genus Psychrobacter comprises 41 validly described species [8]. The structurestructure ofof polysaccharides polysaccharides associated associated with with the cellthe wallcell ofwall bacteria of bacteria of the genus of thePsychrobacter genus Psychrobacterhas not been studiedhas not intensively.been studied To intensively. date, only twoTo date, O-specific only two polysaccharide O-specific polysaccharide structures from structuresP.muricolla T T from2pS P.[9 ]muricolla and P. cryohalolentis 2pST [9] and K5P. cryohalolentis[10], and two K5T capsular [10], and polysaccharidetwo capsular polysaccharide structures from structuresP. arcticus from273-4 P. [11 arcticus] and P. 273 maritimus-4 [11] and3pS P. [ 12maritimus] have been 3pS [ reported.12] have been reported. InIn this this paper, paper, we we report report on on the the isolation, isolation, purification purification,, and and structure structure of the of CPS the produced CPS produced by P. by T P.marincola marincola KMMKMM 277 277T, isolated, isolated from from the homogenized the homogenized internal internal tissues tissues of an ofascidian an ascidian PolysyncratonPolysyncraton sp. [sp.13]. [ 13It was]. It found was found that the that CPS the is a CPS branched is a branched high-molecular high-molecular-weight-weight polymer that polymer effectively that inhibits effectively theinhibits viability the viabilityand colony and formation colony formation of HL-60 ofcells HL-60. cells. 2. Results Results 2.1. Isolation, Isolation, P Purification,urification, and and G Generaleneral C Characterizationharacterization of ofthe the CPS CPS AAnn experimentexperiment usingusing transmission transmission electron electron microscopy microscopy showed showed the presencethe presence of a capsularof a capsular structure T structurearound P. around marincola P. KMMmarincola 277 KMMcells [13277].T Thecells dried [13]. bacterialThe dried cells bacterial were subjected cells were to extractionsubjected to with extractionsodium chloride with sodium solution chloride followed solution by enzymatic followed treatment. by enzymatic The CPS treatment. from the resultingThe CPS materialfrom the was purifiedresulting by material ultracentrifugation was purified followed by ultracentrifugation by anion-exchange followed chromatography by anion-exchange and gel chromatography filtration. Analysis andof the gel CPS filtration revealed. Analysis no contaminant of the CPS proteins revealed and no fatty contaminant acids. The sizeproteins exclusion and fatty chromatography acids. The size (SEC) exclusionanalysis showed chromatography that the CPS (SEC) forms analysis a single showed symmetrical that the CPS peak forms and a has single a molecular symmetrical weight peak of and about 106.9has a molecular kDa (Figure weight1a). The of about electrophoretic 106.9 kDa (Fig profileure 1a of). the The CPS electrophoretic showed a broad profile smear, of the limited CPS showed from 55 (top)a broad to 26smear, kDa limited (Figure from1b). 55 (top) to 26 kDa (Figure 1b). (a) (b) Figure 1. 1. ((aa)) HPSEC HPSEC elution elution profile profile of of the the CPS CPS from from P.P. marincola marincola KMMKMM 277 277T andT and dextran dextran standards standards (insert)(insert);; ( (bb)) Alcian Alcian blue blue-stained-stained electrophoregram electrophoregram of of the the CPS CPS from from P.P. marincola marincola KMMKMM 277 277T. T. Mar. Drugs 2020, 18, 268 3 of 17 Mar. Drugs 2020, 18, x 3 of 17 MonosaccharideMonosaccharide analysisanalysis using using GC-MS GC-MS of theof acetylatedthe acetylated alditols alditols and acetylated and acetylated methyl glycosides methyl glycosides(Figure2) disclosed (Figure the2) disclosed presence of the ribose, presence glucose, of glucosamine,ribose, glucose, and glucosamine galactosamine, and uronic galactosamine acid, all with uronicthe D configurationacid, all with [the14,15 D]. con Furtherfiguration study [14,
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